Unveiling the Evolutionary History of cis-Andean Alouatta (Atelidae, Alouattinae) Through Mitochondrial Genomes

Abstract

Alouatta, a genus widely distributed throughout South and Central America, displays remarkable species diversity across various morphoclimatic domains. To clarify the ancestral distribution and its role in the radiation of Alouatta, our study employed time-tree phylogenetic analyses to better understand the current distribution patterns of the cis-Andean species. We generated 36 mitogenomes, including a species and representatives of populations not previously analyzed, to reconstruct a molecular-dated tree, estimate genetic distance-based analyses, and infer the ancestral distribution range of Alouatta. Our study suggests an initial split within the Alouatta during the Miocene, leading to the separation of the cis-Andean and trans-Andean clades. Through ancestral range reconstruction, we found that the most recent common ancestor of Alouatta was broadly distributed across South America. Within the cis-Andean clade, two major splits were identified. One split revealed a close relationship between the Amazonia-endemic species A. seniculus and A. caraya, a species adapted to open-dry domains, with ancestral range in the Amazonia and dry-open domains. In contrast, for the A. guariba and A. belzebul groups, which occur in Amazonia and the Atlantic Forest, the ancestral range included both domains. The diversification of the Alouatta was driven by two cladogenesis events. The formation of the extant species was primarily driven by founder events during the Pleistocene and involved long-distance dispersal events with posterior population isolation. These events played a crucial role in the formation of new populations that underwent rapid divergence, resulting in distinct phylogenetic lineages. Our findings shed new light on the origins of cis-Andean lineages of Alouatta across a broad geographic range, as well as the emergence of more recent taxa during the Pleistocene. This provides insights into their relationships, highlighting the crucial role of Pleistocene climatic changes and founder events in shaping the diversification and geographic distribution of extant species.